Substrate specificity and products of side‐reactions catalyzed by jasmonate:amino acid synthetase (JAR1)

Guranowski, Andrzej; Miersch, Otto; Staswick, Paul E.; Suza, Walter; Wasternack, Claus

doi:10.1016/j.febslet.2007.01.049

Cited by 69 publications

(47 citation statements)

References 37 publications

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“…Our structural data show that recruiting less favorable amino acids may interfere with the ability of ATP to bind to FIN219. These results corroborate the results of gas chromatography-mass spectrometry quantification of JA derivatives: In Arabidopsis seedlings, JA-Ile predominates (15,41). Further research is required to identify whether FIN219 has a specific recognition motif for amino acid selectivity.…”

Section: Discussionsupporting

confidence: 84%

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Structural basis of jasmonate-amido synthetase FIN219 in complex with glutathione S-transferase FIP1 during the JA signal regulation

Chen

Kuo

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Far-red (FR) light-coupled jasmonate (JA) signaling is necessary for plant defense and development. FR insensitive 219 (FIN219) is a member of the Gretchen Hagen 3 (GH3) family of proteins in Arabidopsis and belongs to the adenylate-forming family of enzymes. It directly controls biosynthesis of jasmonoyl-isoleucine in JA-mediated defense responses and interacts with FIN219-interacting protein 1 (FIP1) under FR light conditions. FIN219 and FIP1 are involved in FR light signaling and are regulators of the interplay between light and JA signaling. However, how their interactions affect plant physiological functions remains unclear. Here, we demonstrate the crystal structures of FIN219-FIP1 while binding with substrates at atomic resolution. Our results show an unexpected FIN219 conformation and demonstrate various differences between this protein and other members of the GH3 family. We show that the rotated C-terminal domain of FIN219 alters ATP binding and the core structure of the active site. We further demonstrate that this unique FIN219-FIP1 structure is crucial for increasing FIN219 activity and determines the priority of substrate binding. We suggest that the increased FIN219 activity resulting from the complex form, a conformation for domain switching, allows FIN219 to switch to its high-affinity mode and thereby enhances JA signaling under continuous FR light conditions. jasmonate response | far-red light | signaling cross-talk | adenylation enzyme | phytohormone F ar-red (FR) insensitive 219 (FIN219) (1), also known as jasmonate (JA) resistant 1 (JAR1; AtGH3.11) (2), is a member of the auxin-regulated Gretchen Hagen 3 (GH3) family of proteins (3). The GH3 family in Arabidopsis is composed of 19 distinct proteins and is also conserved in plants such as rice (4-6), tomato (7,8), and maize (9), with 13, 15, and 13 members, respectively. Phylogenetically, the GH3 family is classified as part of the adenylate-forming enzyme superfamily, which contains proteins such as firefly luciferase-like enzymes (10). This diverse group of enzymes catalyzes the addition of AMP to carboxyl groups on a wide variety of substrates and typically contains three conserved motifs that form a binding pocket for ATP and AMP substrate intermediates (11). GH3 proteins regulate the activity of plant hormones through amino acid conjugation and have a substantial effect on plant metabolism and physiology (12). For example, FIN219 catalyzes the conjugation of isoleucine (Ile) to JA, forming jasmonoyl-isoleucine (JA-Ile). This reaction results in the degradation of the transcriptional repressor JA-ZIM (zinc-finger protein expressed in inflorescence meristem) domain (JAZ) proteins and the subsequent activation of downstream transcriptional responses (13).FIN219 has been identified in suppressor screenings using a temperature sensitive constitutive photomorphogenic 1 (cop1) mutant line. It is involved in FR light-mediated inhibition of hypocotyl elongation and regulates light inactivation of COP1 activity (1). Furthermore, FIN219 acts as a ...

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Section: Discussionsupporting

confidence: 84%

“…Overexpression of FIN219 causes a FR-specific hyperphotomorphogenic response. During JA signaling, FIN219 catalyzes the conjugations between JA and various amino acids, such as leucine (JA-Leu), valine (JA-Val), or methionine (JA-Met) (15). The fin219 mutants also have a reduced JA-Ile production and JA response (16).…”

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confidence: 99%

Structural basis of jasmonate-amido synthetase FIN219 in complex with glutathione S-transferase FIP1 during the JA signal regulation

Chen

Kuo

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…46 Initial work on AtGH3-11 (JAR1) demonstrated that it catalyzes the formation of JA-Ile. 47 Subsequent studies of the Arabidopsis group II AtGH3-2, -3, -4, -5, -6 and -17 show that these enzymes…”

Section: The Gh3 Family: a Common Gene Family In Plantsmentioning

confidence: 99%

Modulating plant hormones by enzyme action

Westfall

Herrmann

Chen

et al. 2010

Plant Signaling & Behavior

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“…TCP4-regulated LOX2 catalyzes an early step of JA biosynthesis (Gfeller et al, 2010). Lastly, JASMONATE RESISTANT1 (JAR1) functions in the synthesis of biologically active JA-Ile (Guranowski et al, 2007). All four tested genes (TCP4, LOX2, MYC2, and JAR1) were significantly up-regulated in ago1-27 cotyledons (Fig.…”

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confidence: 93%

The Mechanistic Underpinnings of anago1-Mediated, Environmentally Dependent, and Stochastic Phenotype

2016

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98195-5065 (G.A.M., T.L., C.Q.)The crucial role of microRNAs in plant development is exceedingly well supported; their importance in environmental robustness is studied in less detail. Here, we describe a novel, environmentally dependent phenotype in hypomorphic argonaute1 (ago1) mutants and uncover its mechanistic underpinnings in Arabidopsis (Arabidopsis thaliana). AGO1 is a key player in microRNA-mediated gene regulation. We observed transparent lesions on embryonic leaves of ago1 mutant seedlings. These lesions increased in frequency in full-spectrum light. Notably, the lesion phenotype was most environmentally responsive in ago1-27 mutants. This allele is thought to primarily affect translational repression, which has been linked with the response to environmental perturbation. Using several lines of evidence, we found that these lesions represent dead and dying tissues due to an aberrant hypersensitive response. Although all three canonical defense hormone pathways (salicylic acid, jasmonate, and jasmonate/ethylene pathways) were up-regulated in ago1 mutants, we demonstrate that jasmonate perception drives the lesion phenotype. Double mutants of ago1 and coronatine insensitive1, the jasmonate receptor, showed greatly decreased frequency of affected seedlings. The chaperone HEAT SHOCK PROTEIN 90 (HSP90), which maintains phenotypic robustness in the face of environmental perturbations, is known to facilitate AGO1 function. HSP90 perturbation has been shown previously to upregulate jasmonate signaling and to increase plant resistance to herbivory. Although single HSP90 mutants showed subtly elevated levels of lesions, double mutant analysis disagreed with a simple epistatic model for HSP90 and AGO1 interaction; rather, both appeared to act nonadditively in producing lesions. In summary, our study identifies AGO1 as a major, largely HSP90-independent, factor in providing environmental robustness to plants. ARGONAUTE1 (AGO1) is an ancient, highly conserved essential protein. One of 10 functionally distinct AGO proteins in the plant Arabidopsis (Arabidopsis thaliana), AGO1 uses microRNAs (miRNAs) to decrease the expression of target genes. AGO1 and the miRNA pathway are crucial for many regulatory processes throughout development and in response to environmental stimuli. As frequent components of feedforward loops, miRNAs also play important roles in controlling gene expression noise and maintaining the phenotypic robustness of specific traits in several organisms, including plants ( Lempe et al., 2013).AGO1 and miRNAs also are critical for proper plant responses to abiotic stress. The expression levels of miRNAs respond to heat shock, cold, drought, oxidative stress, UV light exposure, and hypoxia (Sunkar et al., 2012). For example, in response to drought, the expression of miR169 decreases and the expression of its target gene, encoding the transcription factor NFYA5, increases in Arabidopsis (Li et al., 2008). Increased expression of NFYA5 supports plant survival in drought conditions. Transgenic plants ove...

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Substrate specificity and products of side‐reactions catalyzed by jasmonate:amino acid synthetase (JAR1)

Cited by 69 publications

References 37 publications

Structural basis of jasmonate-amido synthetase FIN219 in complex with glutathione S-transferase FIP1 during the JA signal regulation

Structural basis of jasmonate-amido synthetase FIN219 in complex with glutathione S-transferase FIP1 during the JA signal regulation

Modulating plant hormones by enzyme action

The Mechanistic Underpinnings of anago1-Mediated, Environmentally Dependent, and Stochastic Phenotype

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